RESEARCH ARTICLE

The Association Between Asthma and Sleep in Urban Adolescents With Undiagnosed Asthma DAPHNE KOINIS MITCHELL, PhDa SHERYL J. KOPEL, MScb BRITTNEY WILLIAMS, BAc AMARILIS CESPEDES, MPHd JEAN-MARIE BRUZZESE, PhDe

ABSTRACT BACKGROUND: We examined associations between asthma and sleep in a sample of inner-city adolescents with asthma-like symptoms who are undiagnosed, and to assess the extent to which youth’s report of perceived stress moderates this association. METHODS: A total of 349 adolescents (83% girls), with a mean age of 15.8 years, and their primary caregivers participated. Large segments of the sample were Latinos (46%) or African Americans (37%). Adolescents reported on asthma—namely, rate of waking up at night due to asthma-like symptoms and perceived severity of breathing problems—and sleep, specifically sleep-wake behavior problems and daytime sleepiness during activities. Caregivers provided demographic information by telephone. RESULTS: Night awakenings and perceived severity of breathing problems were each independently associated with sleep-wake behavior problems and daytime sleepiness during activities. Youth report of perceived stress moderated the association between perceived severity of breathing problems and sleep-wake behavior problems, and perceived severity of breathing problems and daytime sleepiness during activities. CONCLUSIONS: Results suggest the importance of interventions that consider undiagnosed asthma and its effects on sleep indicators related to daytime functioning in this high risk group of youth. This study highlights the need for interventions that consider asthma severity, nocturnal asthma, and sleep problems among urban adolescents with no asthma diagnosis. Keywords: asthma-like symptoms; undiagnosed asthma symptoms; adolescents, urban health. Citation: Mitchell D, Kopel SJ, Williams B, Cespedes A, Bruzzese J-M. The association between asthma and sleep in urban adolescents with undiagnosed asthma. J Sch Health. 2015; 85: 519-526. Received on March 28, 2014 Accepted on January 12, 2015

A

sthma prevalence rates continue to escalate among urban youth,1 with rates greater than 20% being reported.2 African American and Latino children are disproportionately affected with greater disease prevalence compared with their non-Latino White (NLW) counterparts.3 Urban youth diagnosed with asthma experience greater asthma morbidity, including activity restriction and sleep disruption, and a number of multilevel factors—such as disease

severity, poverty, acculturative stress, exposure to allergens and irritants, and insurance status—are implicated.4-7 Undiagnosed Asthma Among Urban Adolescents: An Understudied Group at Further Risk Research with 7- to 18-year-olds indicates that 28% to 50% of those with asthma-like symptoms lack an asthma diagnosis, and therefore, are underdiagnosed

a

Research Associate Professor, ([email protected]), Bradley/Hasbro Children’s Research Center, Warren Alpert Medical School of Brown University, 1 Hoppin Street, Providence, RI 02903. bResearch Associate, ([email protected]), Bradley/Hasbro Children’s Research Center, Warren Alpert Medical School of Brown University, 1 Hoppin Street, Providence, RI 02903. c Research Assistant, ([email protected]), Bradley/Hasbro Children’s Research Center, Warren Alpert Medical School of Brown University, 1 Hoppin Street, Providence, RI 02903. dProject Director, ([email protected]), Department of Child and Adolescent Psychiatry, Child Study Center, New York University School of Medicine, One Park Avenue 7th FL, New York, NY 10016. e Associate Professor, ([email protected]), New York University School of Medicine, Child Study Center, One Park Avenue 7th FL, New York, NY 10016. Address correspondence to: Jean-Marie Bruzzese, Associate Professor, ([email protected]), New York University School of Medicine, Child Study Center, One Park Avenue 7th FL, New York, NY 10016. This work was supported by the National Heart, Lung and Blood Institute (R01HL089493 to J.M.B). The authors have no conflicts of interests to disclose.

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or undertreated.2,8-10 Undiagnosed and untreated asthma can result in significant activity limitation, loss of school days, and in cases where symptoms are more severe and dangerous, the need for emergent care.8,10-12 In fact, among those with moderate to severe persistent symptoms, diagnosed and undiagnosed youth experience equally high rates of daytime and nighttime symptoms and asthmarelated activity limitation and school absences.8,11,12 Adolescents are an especially vulnerable group because many have frequent asthma-like symptoms,8-10 have greater asthma morbidity due to asthma symptoms,8,11 and inconsistently utilize healthcare services.10,11,13 It also has been shown that adolescents are more prone to shorter sleep duration and poor sleep habits.14,15 Focusing on adolescent youth is critical as many health-related behavioral patterns that are formed during adolescence continue in adulthood and affect adult health outcomes.15,16 Children’s Sleep: An Important Avenue for Intervention in Youth With Asthma-Like Symptoms Children with poorly controlled asthma-like symptoms may have difficulty initiating or maintaining sleep due to nocturnal symptoms which can make them more vulnerable to poor sleep quality.17-20 In a study including children with diagnosed asthma and healthy controls, a higher number of night awakenings has been found in children with asthma compared with those without asthma.21 Sleep disruption due to nocturnal asthma-like symptoms also may occur more often in children with persistent asthma than in those with intermittent asthma,22 because their increased severity may increase the frequency of nighttime symptoms. Frequent night awakenings in youth with diagnosed asthma can result in poor sleep quality and can affect daytime alertness,23 increased school absences,24 poorer school performance,25 increased risk for behavior problems,26 and poor quality of life.27,28 Research to date in this area has included youth either with a physician diagnosis of asthma confirmed directly or by parent report; this relationship was yet to be studied in adolescents with asthma-like symptoms who lack a diagnosis, a highly vulnerable group. Stressors Relevant to Urban Youth With Asthma Urban ethnic minority children with asthma-like symptoms are more vulnerable to neighborhood and family-level stress, and this can affect their susceptibility to asthma symptoms.29 Urban stressors and low-income status are also shown to be associated with poor sleep quality in children in other disease groups.30 Understanding the extent to which perceptions of stress affect the link between 520 •

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asthma and sleep in vulnerable samples, such as urban adolescents with asthma-like symptoms and no diagnosis, may help to identify modifiable factors and provide important opportunities for intervention across multiple settings where students spend the majority of their time, such as at home and/or school. The Current Study This study examines the association between asthma and sleep behaviors in a group of urban adolescent students with undiagnosed asthma. Asthmarelated indicators include adolescents’ report of night awakenings due to breathing problems, and their perceived severity of breathing problems/asthma-like symptoms. Each of these indicators is utilized in the assessment of asthma morbidity in urban children.17 Sleep-related indicators include the youth’s report of their sleep-wake behavior problems and the level of daytime sleepiness during activities. These sleep indicators have been used in several studies assessing sleep in adolescents and have been shown to correlate with indicators of daytime functioning, such as concentration.14 We hypothesized that more frequent adolescent reported night awakenings and higher levels of perceived severity of breathing problems would each be associated with reports of more sleep-wake behavior problems and daytime sleepiness. In addition, we examined whether perceived stress moderated the association between asthma-like symptoms and sleep indicators in this group. We expected that asthma-like symptoms and sleep behaviors would be more strongly associated in the context of higher levels of perceived stress.

METHODS Design and Procedures Data for this cross-sectional analysis are drawn from the baseline visit of a larger, randomized clinical trial examining the efficacy of a school-based intervention, Asthma Self-Management for Adolescents with Undiagnosed Asthma (ASMA-Undx), which aims to assist high school students who meet criteria for moderate to severe persistent asthma, but who are yet to be diagnosed, obtain a clinical evaluation, and a diagnosis and treatment, if warranted.31 Eligible students were drawn from 40 schools in neighborhoods with elevated rates of asthma hospitalizations; schools also needed to have no other ongoing asthma interventions To determine eligibility for the clinical trial, all students in grades 9 to 11 completed 2 brief validated asthma case detection surveys,2,32 which allowed the investigators to determine whether or not students

© 2015, American School Health Association

had probable asthma, the level of severity of their asthma-like symptoms based on NHLBI categories for severity of symptoms,17 and if they were ever diagnosed with asthma. Trained project staff obtained written assent and informed consent from eligible students, which were those with probable moderate to severe persistent asthma and no diagnosis, to participate in the clinical trial. Exclusion criteria included having other comorbid diseases that might impact lung functioning and/or highly specialized developmental or learning needs. The student baseline assessment consisted of surveys that were independently completed by each student, as well as interviews by trained project staff; students’ primary caregivers were interviewed by telephone by trained project staff.

Instrumentation Participant characteristics. Students provided their sex, date of birth, and race/ethnicity. Primary caregivers reported on their highest level of education and employment status. Asthma-related indicators. Students completed 2 asthma measures used in prior research examining asthma morbidity in urban youth with diagnosed and undiagnosed asthma.17,31,33-35 First, they reported the number of night awakenings due to asthma-like symptoms that they experienced in the prior 2 weeks. Next, students indicated the perceived severity of their asthma-like symptoms by indicating on a 5-point Likert scale how much they were bothered overall in the last 2 weeks by breathing problems, with 0 = Not bothered to 4 = Very bothered. Sleep-related indicators. Students answered several questions related to sleep behaviors and sleepiness from the School Sleep Habits Survey (SSHS),14,36 a widely used survey with good psychometric properties with urban adolescents. Students completed the SleepWake Behavior Problems Scale, which consists of 15 items regarding the frequency of erratic sleep/wake behaviors over the prior 2 weeks using a 5-point Likert scale, with 0 = Never to 4 = Every day/night. Sample items include: feeling satisfied with your sleep and falling asleep in a morning or afternoon class. To assess daytime sleepiness, students answered a single question regarding how much of a problem they have with sleepiness during daytime activities, using a 5point Likert scale, with 0 = Not a problem at all, to 4 = A very big problem. Perceived stress. Students completed the 4-item Perceived Stress Scale (PSS-4),37,38 which measures the degree to which youth feel their lives were unpredictable, uncontrollable, and overwhelming in the preceding month. Items are scored on a 5-point Likert scale, with 0 = Never through 4 = Very often. Journal of School Health



This scale has been widely used with adolescents with adequate reliability reported.39 Data Analysis Preliminary analyses were conducted to examine associations among demographic variables: child age, ethnicity/race, sex, caregiver employment status and caregiver education; asthma indicators: number of night waking and perceived severity of breathing problems; sleep indicators: sleep-wake behavior problems and daytime sleepiness during activities; and perceived stress. We used Pearson’s correlations when both variables were continuous, or analyses of variance (ANOVA) when examining continuous variables across discrete groups, such as sex or race/ethnic group. Chi square analyses helped to assess relationships for categorical variables. We then examined the association between each asthma-related indicator—the predictor—and each sleep indicator—the dependent variable—in 4 hierarchical, linear regression analyses. Demographic variables that could represent potential confounds were controlled, when appropriate, as indicated by preliminary analyses. Next, we examined the moderational role of perceived stress in the association between asthma and sleep. In each hierarchical regression moderation model, the demographic variable was entered into the regression equation in the first step, when appropriate. In the second and third steps, the 2 variables representing potential main effects—perceived stress and each asthma indicator, respectively—were entered. This was followed in the last step by the interaction term of perceived stress and the asthma indicator. We conducted post hoc probing to clarify interaction terms that were statistically significant or represented statistical trends, as in our previous work.40 The relationships between asthma and sleep indicators were tested in the context of high and low levels of perceived stress, as determined by a median split.40 Statistical significance was judged at p < .05, which was used for all statistical tests; trends with p < .10 are also reported for descriptive purposes. Effect sizes for analyses of variance were expressed as partial omega squared (ω2 p ), which are interpreted as small (.01), medium (.06) or large (.14).41 R2 adjusted are presented for multiple regression results. Statistical analyses were performed using SPSS version 12 (SPSS, Inc., Chicago, IL).

RESULTS Table 1 provides a summary of demographic information, baseline clinical characteristics, and the distribution of asthma, sleep and stress variables for the sample.

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Table 1. Demographic and Clinical Characteristics of Student Participants and Caregivers, and Distribution of Predictors and Dependent Variables Demographic and Clinical Characteristics (N = 349)

Table 2. Moderational Model: Predictors of Sleep-Wake Behavior Problems Model R2 adjusted

N (%)

Student characteristics Female Age in years [M (SD)] Ethnicity Latino African American Other Severity of asthma-like symptoms Moderate persistent Severe persistent Primary caregiver characteristics (N= 240) Education Less than high school education Completed high school education Beyond high school education Employment status (n= 239) Full time Part time Home maker Unemployed or laid off Not employed (ie, leave of absence, retired, disability, full-time student)

Night awakenings Perceived stress .16 Number of night awakenings Perceived .15 stress × number of night awakenings Perceived severity of breathing problems Perceived stress .16 Perceived severity of breathing problems Perceived .17 stress × perceived severity

289 (83) 15.8 (1.1) 160 (46) 130 (37) 59 (17) 186 (53) 163 (47)

88 (37) 60 (25) 92 (38)

# Night awakenings, past 2weeks Perceived severity of breathing problems Sleep-wake behavior problems total score Daytime sleepiness during activities Perceived stress total score

M (SD) Range 2.5 (3.5) 0-14 2.2 (1.2) 0-4 18.3 (7.4) 0-37 1.6 (1.1) 0-4 7.5 (2.7) 0-16

Associations Between Asthma and Sleep Indicators Results from separate hierarchical regression analyses controlling for sex when appropriate revealed that the number of night awakenings significantly predicted sleep-wake behavior problems (β = 0.18, •

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p-Value

0.36 0.13

7.25 2.58

The Association Between Asthma and Sleep in Urban Adolescents With Undiagnosed Asthma.

We examined associations between asthma and sleep in a sample of inner-city adolescents with asthma-like symptoms who are undiagnosed, and to assess t...
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